Cellular and molecular characterisation of regeneration in calcareous sponges and soft corals

Abstract

Regeneration, the ability to replace damaged or lost body parts, is widespread but highly variable across animals, indicating a complex evolutionary history. Studying animals representing early-branching lineages offers unique insights into the fundamental mechanisms and the evolutionary trajectory of this fascinating trait. This thesis investigates the regenerative capacities of soft corals from the genus Xenia and calcareous sponges from the genus Sycon. Cnidarians, which include corals, sea anemone, and jellyfish, are renowned for their remarkable regenerative abilities. Occupying a key phylogenetic position as the sister group to Bilateria, cnidarians offer crucial insights into the evolution of animals. This phylum, encompasses a diverse range of species, generally characterised by overt radial symmetry and a morphologically simple, diploblastic body plan. The soft coral Xenia (Octocorallia) is a prevalent and resilient genus in the shallow waters of Indo-Pacific coral reefs. Xenia possesses a fleshy body embedded with small, platelet-shaped calcium carbonate sclerites providing structural support and protection. The sclerites are produced by calcium secreting cells called scleroblasts. Sponges, representing one of the earliest branching animal lineages, are known for their morphologically simple yet highly efficient body plans, consisting mainly of two layers of epithelial cells. They are capable of whole-body regeneration and reaggregation from dissociated cells, making them ideal models for studying fundamental regenerative processes. The significance of calcareous sponges lies in their phylogenetic position among the oldest extant animal lineages, their directional apical-to-basal axis morphology, and their extensive gene repertoire. Notably, this is the only sponge class to have calcitic skeletal elements, produced by specialised cell types called sclerocytes. Here, I describe the regeneration process in Xenia from small body fragments and identify differential expression of developmental and putative biomineralisation genes. By integrating these findings with available single-cell RNA-Seq data from Xenia and a stony coral species, I have uncovered the transcriptome of Xenia's previously bioinformatically undetected scleroblasts. This discovery sheds light on the evolutionary origin of scleroblasts from secretory cells and reveals an ancestral biomineralisation cassette. Furthermore, I present evidence suggesting that biomineralisation in both soft and stony corals and calcareous sponges evolved independently. In the proposed evolutionary scenario, each lineage inherited an ancestral organic scaffold and subsequently co-opted a biomineralisation toolkit, enabling the deposition of minerals onto the existing organic scaffold. Skeletogenesis in soft corals and calcareous sponges was acquired by mesohyl/mesoglea cells which form small calcitic elements, whereas in stony corals, it occurred within the aboral ectoderm, forming massive aragonitic skeletons. The analysis of the molecular and cellular mechanisms employed by Xenia and Sycon in response to injury and during wound healing revealed the involvement of an ancient animal wound healing pathway, marked by the activation of the immediate early response genes Jun and Fos. This suggests the presence of a conserved animal injury response pathway, which probably originated in the ancestors of all animals. Insights gained in this thesis offer a window into the evolutionary pathways that have shaped the development, regeneration, and biomineralisation processes in animals.